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Identification of a p53-dependent Negative Response Element in the bcl-2 Gene¹

La Jolla Cancer Research Foundation, Cancer Research Center, La Jolla, California 92037

Recently, we have shown that the p53 tumor suppressor gene product can inhibit expression of the bcl-2 gene. In this report, we explored the molecular basis for p53-mediated down-regulation of bcl-2 gene expression using a cotransfection approach involving p53 expression plasmids and chloramphenicol acetyltransferase (CAT) reporter gene constructs containing regions from the bcl-2 gene. When transfected into a p53-deficient human lung cancer cell line H358, reporter gene constructs containing only the promoter region of bcl-2 and upstream sequences were not suppressed by p53. Inclusion of bcl-2 gene sequences corresponding to the 5' untranslated region in bcl-2/CAT constructs, however, resulted in p53-dependent down-regulation. A 195-base pair segment from the bcl-2 gene 5' untranslated region was found to be capable of conferring p53-dependent repression on a heterologous expression plasmid containing CAT under the control of an SV40 immediate early-region promoter. This p53-negative response element functioned in an orientation-independent manner when placed either upstream or downstream of the SV40-CAT transcription unit. The results demonstrate the existence of a negative response element in the bcl-2 gene through which p53 may either directly or indirectly transcriptionally down-regulate expression of this gene involved in the regulation of programmed cell death.

¹ Supported by National Cancer Institute Grant CA-60181 and by Grant DHP32C from the American Cancer Society. J. C. R. is a Scholar of the Leukemia Society of America.

² To whom requests for reprints should be addressed, at La Jolla Cancer Research Foundation, Cancer Research Center, 10901 N. Torrey Pines Rd., La Jolla, CA 92037.

Received 4/ 6/94. Accepted 5/12/94.

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				Y. Sun, Y. Sun, L. Wenger, J. L. Rutter, C. E. Brinckerhoff, and H. S. Cheung p53 Down-regulates Human Matrix Metalloproteinase-1 (Collagenase-1) Gene Expression J. Biol. Chem., April 23, 1999; 274(17): 11535 - 11540. [Abstract] [Full Text] [PDF]

				A. Leri, Y. Liu, X. Wang, J. Kajstura, A. Malhotra, L. G. Meggs, and P. Anversa Overexpression of Insulin-Like Growth Factor-1 Attenuates the Myocyte Renin-Angiotensin System in Transgenic Mice Circ. Res., April 16, 1999; 84(7): 752 - 762. [Abstract] [Full Text] [PDF]

				M. Nozaki, M. Tada, H. Kobayashi, C.-L. Zhang, Y. Sawamura, H. Abe, N. Ishii, and E. G. Van Meir Roles of the functional loss of p53 and other genes in astrocytoma tumorigenesis and progression Neuro-oncol, April 1, 1999; 1(2): 124 - 137. [Abstract] [PDF]

				A. Leri, Y. Liu, P. P. Claudio, J. Kajstura, X. Wang, S. Wang, P. Kang, A. Malhotra, and P. Anversa Insulin-Like Growth Factor-1 Induces Mdm2 and Down-Regulates p53, Attenuating the Myocyte Renin-Angiotensin System and Stretch-Mediated Apoptosis Am. J. Pathol., February 1, 1999; 154(2): 567 - 580. [Abstract] [Full Text] [PDF]

				K. J. Townsend, P. Zhou, L. Qian, C. K. Bieszczad, C. H. Lowrey, A. Yen, and R. W. Craig Regulation of MCL1 through a Serum Response Factor/Elk-1-mediated Mechanism Links Expression of a Viability-promoting Member of the BCL2 Family to the Induction of Hematopoietic Cell Differentiation J. Biol. Chem., January 15, 1999; 274(3): 1801 - 1813. [Abstract] [Full Text] [PDF]

				A.R. Kamer, L. Krebs, S.A. Hoghooghi, and C. Liebow Proliferative and Apoptotic Responses in Cancers With Special Reference To Oral Cancers Critical Reviews in Oral Biology & Medicine, January 1, 1999; 10(1): 58 - 78. [Abstract] [Full Text] [PDF]

				F. Aillet, H. Masutani, C. Elbim, H. Raoul, L. Chene, M.-T. Nugeyre, C. Paya, F. Barre-Sinoussi, M.-A. Gougerot-Pocidalo, and N. Israel Human Immunodeficiency Virus Induces a Dual Regulation of Bcl-2, Resulting in Persistent Infection of CD4+ T- or Monocytic Cell Lines J. Virol., December 1, 1998; 72(12): 9698 - 9705. [Abstract] [Full Text] [PDF]

				H.-K. G. Shu, M. M. Kim, P. Chen, F. Furman, C. M. Julin, and M. A. Israel The intrinsic radioresistance of glioblastoma-derived cell lines is associated with a failure of p53 to induce p21BAX expression PNAS, November 24, 1998; 95(24): 14453 - 14458. [Abstract] [Full Text] [PDF]

				G. Evan and T. Littlewood A Matter of Life and Cell Death Science, August 28, 1998; 281(5381): 1317 - 1322. [Abstract] [Full Text]

				S. Ambs, M. O. Ogunfusika, W. G. Merriam, W. P. Bennett, T. R. Billiar, and C. C. Harris Up-regulation of inducible nitric oxide synthase expression in cancer-prone p53 knockout mice PNAS, July 21, 1998; 95(15): 8823 - 8828. [Abstract] [Full Text] [PDF]

				M. D. Smith, E. A. Ensor, R. S. Coffin, L. M. Boxer, and D. S. Latchman Bcl-2 Transcription from the Proximal P2 Promoter Is Activated in Neuronal Cells by the Brn-3a POU Family Transcription Factor J. Biol. Chem., July 3, 1998; 273(27): 16715 - 16722. [Abstract] [Full Text] [PDF]

				B. A. Froesch, S. Takayama, and J. C. Reed BAG-1L Protein Enhances Androgen Receptor Function J. Biol. Chem., May 8, 1998; 273(19): 11660 - 11666. [Abstract] [Full Text] [PDF]

				N. A. Jones, J. Turner, A. J. McIlwrath, R. Brown, and C. Dive Cisplatin- and Paclitaxel-Induced Apoptosis of Ovarian Carcinoma Cells and the Relationship between Bax and Bak Up-Regulation and the Functional Status of p53 Mol. Pharmacol., May 1, 1998; 53(5): 819 - 826. [Abstract] [Full Text]

				J. T Colston, B. Chandrasekar, and G. L Freeman Expression of apoptosis-related proteins in experimental coxsackievirus myocarditis Cardiovasc Res, April 1, 1998; 38(1): 158 - 168. [Abstract] [Full Text] [PDF]

				C. A. Pise-Masison, K.-S. Choi, M. Radonovich, J. Dittmer, S.-J. Kim, and J. N. Brady Inhibition of p53 Transactivation Function by the Human T-Cell Lymphotropic Virus Type 1 Tax Protein J. Virol., February 1, 1998; 72(2): 1165 - 1170. [Abstract] [Full Text] [PDF]

				A. Leri, Y. Liu, A. Malhotra, Q. Li, P. Stiegler, P. P. Claudio, A. Giordano, J. Kajstura, T. H. Hintze, and P. Anversa Pacing-Induced Heart Failure in Dogs Enhances the Expression of p53 and p53-Dependent Genes in Ventricular Myocytes Circulation, January 20, 1998; 97(2): 194 - 203. [Abstract] [Full Text] [PDF]

				A. Sablina, G. Ilyinskaya, S. Rubtsova, L. Agapova, P. Chumakov, and B. Kopnin Activation of p53-mediated cell cycle checkpoint in response to micronuclei formation J. Cell Sci., January 4, 1998; 111(7): 977 - 984. [Abstract] [PDF]

				V. Levresse, A. Renier, J. Fleury-Feith, F. Levy, S. Moritz, C. Vivo, Y. Pilatte, and M.-C. Jaurand Analysis of Cell Cycle Disruptions in Cultures of Rat Pleural Mesothelial Cells Exposed to Asbestos Fibers Am. J. Respir. Cell Mol. Biol., December 1, 1997; 17(6): 660 - 671. [Abstract] [Full Text]

				W. R. MacLellan and M. D. Schneider Death by Design : Programmed Cell Death in Cardiovascular Biology and Disease Circ. Res., August 19, 1997; 81(2): 137 - 144. [Abstract] [Full Text]

				C. Heckman, E. Mochon, M. Arcinas, and L. M. Boxer The WT1 Protein Is a Negative Regulator of the Normal bcl-2 Allele in t(14;18) Lymphomas J. Biol. Chem., August 1, 1997; 272(31): 19609 - 19614. [Abstract] [Full Text] [PDF]

				T. M. Nork, G. L. Poulsen, L. L. Millecchia, R. G. Jantz, and R. W. Nickells p53 Regulates Apoptosis in Human Retinoblastoma Arch Ophthalmol, February 1, 1997; 115(2): 213 - 219. [Abstract] [PDF]

				M Murphy, A Hinman, and A J Levine Wild-type p53 negatively regulates the expression of a microtubule-associated protein. Genes & Dev., December 1, 1996; 10(23): 2971 - 2980. [Abstract] [PDF]

				L. Klampfer, J. Zhang, A. O. Zelenetz, H. Uchida, and S. D. Nimer The AML1/ETO fusion protein activates transcription of BCL-2 PNAS, November 26, 1996; 93(24): 14059 - 14064. [Abstract] [Full Text] [PDF]

				H. Xiang, D. W. Hochman, H. Saya, T. Fujiwara, P. A. Schwartzkroin, and R. S. Morrison Evidence for p53-Mediated Modulation of Neuronal Viability J. Neurosci., November 1, 1996; 16(21): 6753 - 6765. [Abstract] [Full Text] [PDF]